Tuesday, September 27, 2011

I recently attended a workshop on Cultural Niche Construction organized by Kevin Laland and Mike O’Brien. About 15 researchers gathered at the Konrad Lorenz Institute, just outside Vienna, Austria, to discuss a variety of topics related to Niche Construction Theory (NCT). As described in Post & Palkovacs 2009, NCT is similar to eco-evolutionary dynamics in that it recognizes the bi-directional interactions between the environmental modification caused by populations and the subsequent evolution of that (and other) populations. Some subtle differences in emphasis and terminology exist between eco-evolutionary dynamics (as studied by evolutionary ecologists) and NCT (as studied by animal behaviorists and anthropologists), and these differences generated much lively discussion.

After ironing out our differences (or deciding to shelve them so we could move along), the main topic of the meeting focused on the role of culture in shaping the ecology and evolution of animals and humans. Talks covered a huge variety of fascinating topics, including ecosystem engineering, social structure, tool use, and the origins of agriculture and public health institutions. In one fascinating example, crows from the island of New Caledonia have learned to use tools to obtain food in the wild and solve a variety of puzzles contrived by researchers. This culturally transmitted ability to make and use tools appears to have shaped the evolution of beak morphology in this species. And human evolution has undoubtedly been impacted by cultural practices. One example is the domestication of plants and animals, which emerged as a shared arena of interest for those focused on the evolution of humans, those focused on the genetics of domestication, and those (like myself) focused on the broader ecological implications of domestication as a special case of human-induced evolution.

This project started with a PhD summer school in 2009 at the Centre forEcology, Evolution and Biogeochemistry, in Kastanienbaum Switwerland(Eawag CEEB). We recruited an all-star cast of lecturers that had a broad interest in eco-evolutionary dynamics, including: Jim Elser, Nelson Hairston Jr., Eric Triplett, Andrew Hendry, Elena Litchman, and Luc De Meester. For two weeks they regaled us (seeparticipants) with their stories, and inspired us to put something down on paper.

Our starting point was a paper by Jim Elser in The American Naturalist(Biological Stoichiometry: A Chemical Bridge between Ecosystem Ecology and Evolutionary Biology). This paper called for a unification of evolutionary thinking with ecosystem ecology and labelled this challenge "the most important frontier for biological integration".

Several sub-disciplines have taken up this challenge, including biodiversity andecosystem functioning research, ecological speciation, and communitygenetics. Moving forward, I think the growing field of eco-evolutionarydynamics can make a substantial contribution to this effort.

To make progress, we need to identify heritable traits that underlie theeffects organisms have on their ecosystems. If such traits are also a targetof natural selection, then phenotypic evolution might have predictableconsequences for ecosystem processes. This sounds easy enough, but todo this we need to make 'interdisciplinary research' much less of a buzzword,and more of a working reality.

Some of the best examples of integration between evolutionary biology andecosystem science have come from recent manipulative field and mesocosmexperiments. In this review, we have branded such experiments as "commongardening experiments", to emphasize that organisms differ in how theymodify (or garden) their environment. So far, one in three reviewersdoesn't like this term, but we think it's useful.

Common gardening experiments bring researchers together from disparate disciplines. If you look at the authors lists of papers like Palkovacs et al. 2009 PTRS-B , Harmon et al. 2009 Nature , Bassar et al. 2010 PNAS , you will see a refreshing mix of researchers with backgrounds in both evolutionary biology and ecosystem science. These papers provide some initial proof-of-concept, but really only scratch the surface of the rich role that evolution can play in our natural ecosystems.

Saturday, September 17, 2011

In science, it is both boring and annoying when everyone agrees. Once that happens, what is there to talk about? That is why every working group, talk, or paper needs a Devil’s Advocate. Devil’s Advocates make things exciting. They make things move. They break a discussion or project out of lethargy and complacency, and they cause everyone to crystallize their arguments and ideas and explore new ground. Where would we be without them?

But what if there were too many? What if everyone was a Devil’s Advocate? What would happen then? Maybe nothing. Maybe everyone would be too critical and nothing would move forward. Maybe everything would bog down and nothing would get achieved. That is why every working group, talk, and paper also needs a God’s Advocate. A God’s Advocate sticks behind an idea, selling it to sceptics, and fighting the Devils’ Advocates to some middle ground – a place where progress is made in some new area and is backed with the best possible logic and clarity.

Just a few weeks ago at Gault Nature Reserve on Mt. St. Hilaire, we convened the second meeting of the Quebec Centre for Biodiversity Science (QCBS) working group on Eco-evolutionary Dynamics. (For a dispatch from the whisky-soaked first meeting, see http://ecoevoevoeco.blogspot.com/2011/01/whisky-rescue.html) The main goal of this meeting was to figure out how quickly ecological function evolves. It is now well known that traits can evolve quickly, although they don't always do so, and that some such changes can have ecological effects – but how common is this and on what time scales does it play out? To this end, we compiled databases that examined how quickly ecological function evolves. A few such datasets exist but they aren’t common, and so we also sought to determine rates of change in traits likely to have ecological function, such as body size or trophic position. Jonathan brought his carnivores, Bea and Nicholas brought their zooplankton, Chris and Eric P brought their fish, Hans brought his dinosaurs (what else), Nash and Mark brought their plants, Andrew and Mart brought their contemporary evolution, Fanie and Eric V brought their R and found some birds, Matt brought his model, Gregor brought his Matlab, and David even brought a manuscript!

It turns out that traits evolve – duh - all types of them and at all sorts of different rates. One pattern in particular emerges in almost every dataset: changes can be rapid over short time frames but don’t continue to accumulate into large changes on longer time frames. Kind of like a ball bouncing around in a closed room – fast in any given direction until it hits a wall and then fast in another direction. This isn’t a new result, of course, and so what should we do then? How can we make an important contribution to eco-evolutionary dynamics and go beyond this already recognized pattern? Here was where the advocates – both Devil’s and God’s – came into play. Ideas were raised and trashed and raised and trashed. Sometimes they rose from the ashes of a previous trashing. Sometimes they were never heard from again. And sometimes they just bounced around in that closed room – never coming to rest, but also never getting anywhere.

To my way of thinking, both types of advocates were critical. We came up with some very original and cool ideas for how to analyze rates of evolution – and we used them to find some perhaps surprising patterns in the data that originally seemed to say the same old thing. The new metrics have their limitations, of course, but which metric doesn’t? And they allow us to think about the problem in new ways. I won’t tip our hand in this blog and I could say this was because that the paper is coming soon to an important journal near you. The truth, however, is that the Devil’s Advocates are still doing their job – and so God’s Advocate must find that ultimate magic that finally lets the ball bounce out of the room and into the wide world. Stay tuned for the third meeting.

Mark was missing from the photo -sorry - but perhaps he was checking out these cool shrooms!

Monday, September 5, 2011

On the steamy shores of Lake Balaton in central Hungary was recently convened the “Niche theory and speciation” workshop, hosted by Geza Meszena, Liz Pasztor, and colleagues. Three days of talks were interspersed with opportunities for discussion and debate. A favourite, or at least convenient, venue for debate was the hotel lounge, with a beer or wine in hand and entertainment provided by retirees tripping the light fantastic on the dance floor while an aging trubidor on a synthesizer played the “classics” suffused with a distinctive Hungarian flavour. Somehow the normally stale debate about sympatry versus allopatry gains a new vitality against the backdrop of whirling gray (or overly black) hair and a tinny synthesized “Ring of Fire.”

So just what are “niches” anyway, aside from some set of conditions that are (or might be) occupied by a particular species? Are they Hutchinsonian, Grinnellian, Eltonian, or other? Are they alpha or beta, fundamental or realized? Are they properties of the organisms, the environment, or both? Can a niche exist without an organism occupying it? To what extent do organisms create or destroy niches for themselves and other organisms? Despite much discussion, no agreement was reached – because the different concepts are differentially useful in different contexts. In the end, however, the truth is – as someone pointed out – that “we can’t define them but we know them when we see them.” With this in mind, we can ask how niches might influence speciation.

For instance, one might ask how critical distinct niches are for speciation. Is speciation is always ecological (adaptive) or can it also be non-ecological (non-adaptive)? Bob Holt was happy to champion the potential importance of non-ecological speciation, whereas many adaptive dynamicists remained sceptical. Nevertheless, at least three talks were given on non-ecological speciation, including two on the “neutral theory of speciation.” (Just when I thought Hubbell’s theory was finally waning, it again rears its unrealistic head.) But to be more honest, the presenters merely wish to explore this theory as an interesting mathematical problem – or as a null model – rather than to assert it really was an important contributor to the diversity of life. And yet, as Michael Kopp pointed out, the pesky theory does often seem to get the right answer (predicting real patterns of biodiversity) even though it is presumably for the wrong reason. So although that neutral stuff is all very elegant, we might as well get back to considering the important thing in the evolution of diversity: niches.

Does increasing competition for one niche favour shifts to new niches – as theory predicts or assumes? Of course it does – right? Well, Christine Parent showed that flour beetles stubbornly refuse to obey the laws of niche theory – no matter how often you explain it to them. Other topics of discussion ranged from the classic and general to the new and specific. On the classic end of things, no meeting on speciation would be complete without an impassioned debate on allopatry versus sympatry versus parapatry. Nearly everyone recognized that sympatric contributions to speciation would be most effective following an initial period of allopatry, which led to Ole Seehausen’s pithy observation that perhaps “allopatry is necessary for sympatric speciation.” And, of course, one always needs a vigorous discussion as to whether or not the terms themselves are even useful. In response to a disparaging comment on this point Jon Bridle, Jim Mallet was clear to assert that what he really meant in his earlier statements was “APPROXIMATELY sympatric” and “APPROXIMATELY allopatric.” A new addition to the lexicon of evolutionary biology?

As for the more specific, I was intrigued to learn that a persistent problem in the theoretical world is whether or not continuous coexistence (essentially a very large number of species that partition themselves very finely along a continuous resource gradient) is possible. And the answer proved to be ... YES ... or NO ... or maybe - depending on who was speaking. But, of course, this is a theoretical question since it never happens in nature, which then contributed to a long discussion on the frequent disconnect between theory and empirical data.

And then there were the two hours a small group of us spent debating Joel Brown’s unified theory of human evolution – this one decidedly not based on a neutral theory. Weaving a beautiful adaptive tale with liberal anecdotes from squirrels, culture, politics, and G functions, Joel constructed a convincing simultaneous explanation for those three traits that among the mammals are unique to humans: high maternal mortality at birth, menopause, and concealed ovulation. At least I think he did.

Thursday, September 1, 2011

I recently spent four days at the meeting of the European Society for Evolutionary Biology (ESEB) in Tubingen, Germany. A pleasant surprise was that the meetings were very eco-evolutionary, at least from the perspective of how ecology drives evolution. Lots of talks were given on ecological speciation, interactions between natural and sexual selection, phenotypic plasticity, and the genetics of adaptation. So I had no shortage of talks that I wanted to attend. At one point, five people I wanted to see were talking simultaneously. As the storm clouds gather over Tubingen, however, what I really want to do in this post is rail against a communication problem between the practitioners of a particular field of study and the rest of the evolutionary community.

A contemporary debate in evolutionary biology, and indeed in biology in general, surrounds the genetic basis for adaptation and speciation. Is adaptation the result of many genes of small effect, as Fisher famously declared, or is it instead the result of relatively few genes of large effect? The many-small view held sway for much of the last fifty years – notwithstanding a number of examples of genes that had large phenotypic effects. More recently, however, increasingly powerful molecular methods have led to a seeming sea-change toward the few-large view. In particular, the discovery and characterization of specific genes with large effects on adaptive phenotypes has led a fair number of biologists to now assert that Fisher is dead in both senses, and that we now finally see the world of adaptation in its true – oligogenic – form. This is nonsense – but I can see where it comes from.

Every time I attend a scientific conference – and this year’s ESEB meeting was no exception – most talks on the genetics of adaptation report a search for THE GENES that determine adaptation: sometimes they find such genes and, if not, become apologists for failing to do so. (And published papers are the same way.) This gives the audience the impression that studying the genetics of adaptation must involve a search for THE gene that underlies divergence in the trait. What is often lost on the audience is that investigators normally screen large number of traits for large effect genes and then specifically choose – for practical reasons – to focus only on those of largest effect. In addition, it is often forgotten that Fisher’s assertions were about ADAPTATION per se, not adaptive TRAITS. In general, adaptation to different environments in nature will involve many traits (life history, morphology, physiology, behaviour) and, even if one or two traits within these classes are indeed mainly oligogenic, those same genes will almost certainly contribute to only a small proportion of the variation in overall ADAPTATION.

As just one example, Rowan Barrett gave an outstanding talk about natural selection on EDA, a gene that strongly influences variation in lateral plate number of stickleback fishes, which differ dramatically in this trait between freshwater and marine populations. This work on EDA, along with Hopi Hoekstra’s work on MC1R in field mice, represent some of the best-characterized effects of a single gene on selection and adaptation in natural animal populations. However, EDA gives a misleading picture of overall adaptation to freshwater. For example, genome scans for evidence of divergent selection across the whole genome (work from the lab of Bill Cresko and others), and studies of gene expression (such as by the groups of Louis Bernatchez and Juha Merila), show that adaptation to freshwater in stickleback clearly involves many – probably hundreds – of genes. Thus, while EDA may explain a substantial fraction of the variation in lateral plates, it will not do so for overall ADAPTATION. And similar data on the polygenic nature of adaptation is accumulating from similar studies of other organisms, such as whitefish, mosquitoes, walkingsticks, and so on.

So every time I hear one of those “THE GENE FOR” talks, I can’t wait to corner the author later at the pub – plenty of those in Tubingen – to ply them with fine ales and regale them with polygenic tales. Recently, I have been able to debate the many and the small with Rowan, Hopi, Katie Peichel, David Kingsley, and Dolph Schluter. It turns out that all of the above points are recognized and embraced by these investigators. That is, people actually studying the genetics of adaptation to divergent environments in nature believe that it involves many genes of small to modest effect. It is just that they are specifically studying only those few of largest effect – and it is much easier to study the genetics of a few traits than of overall adaptation to a given environment.